Placentation in the paca (Agouti paca L) - BDPI USP

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Universidade de São Paulo
Biblioteca Digital da Produção Intelectual - BDPI
Departamento de Cirurgia - FMVZ/VCI
Artigos e Materiais de Revistas Científicas - FMVZ/VCI
2005
Placentation in the paca (Agouti paca L)
Reproductive Biology and Endocrinology. 2005 Feb 28;3(1):9
http://www.producao.usp.br/handle/BDPI/33015
Downloaded from: Biblioteca Digital da Produção Intelectual - BDPI, Universidade de São Paulo
Reproductive Biology and
Endocrinology
BioMed Central
Open Access
Research
Placentation in the paca (Agouti paca L)
Marina Bonatelli1, Anthony M Carter*2, Marcia R Fernandes Machado3,
Moacir F De Oliveira4, Marcelo Cardoso de Lima1 and
Maria Angelica Miglino1
Address: 1Department of Surgery, School of Veterinary Medicine, University of Sao Paulo, Sao Paulo, Brazil, 2Department of Physiology and
Pharmacology, University of Southern Denmark, Odense, Denmark, 3Paulista State University, Jaboticabal, Sao Paulo, Brazil and 4Mossoró
Superior School of Agriculture, Rio Grande do Norte, Brazil
Email: Marina Bonatelli - miglino@usp.br; Anthony M Carter* - acarter@health.sdu.dk; Marcia R
Fernandes Machado - mrfmachd@fcav.unesp.br; Moacir F De Oliveira - mfranco@esam.br; Marcelo Cardoso de Lima - miglino@usp.br;
Maria Angelica Miglino - miglino@usp.br
* Corresponding author
Published: 28 February 2005
Reproductive Biology and Endocrinology 2005, 3:9
doi:10.1186/1477-7827-3-9
Received: 01 December 2004
Accepted: 28 February 2005
This article is available from: http://www.rbej.com/content/3/1/9
© 2005 Bonatelli et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background: The paca is a South American rodent with potential as a commercial food animal.
We examined paca placenta as part of a wider effort to understand the reproductive biology of this
species.
Methods: Thirteen specimens between midgestation and term of pregnancy were studied by light
and transmission electron microscopy.
Results: The placenta is divided into several lobes separated by interlobular trophoblast. Maternal
arterial channels and fetal veins are found at the centre of each lobe. In the labyrinth, maternal
blood flows through trophoblast-lined lacunae in close proximity to the fetal capillaries. The
interhaemal barrier is of the haemomonochorial type with a single layer of syncytiotrophoblast.
Caveolae occur in the apical membrane of the syncytiotrophoblast and recesses in the basal
membrane, but there is no evidence of transtrophoblastic channels. The interlobular areas consist
of cords of syncytiotrophoblast defining maternal blood channels that drain the labyrinth. Yolk sac
endoderm covers much of the fetal surface of the placenta. The subplacenta comprises
cytotrophoblast and syncytiotrophoblast. There are dilated intercellular spaces between the
cytotrophoblasts and lacunae lined by syncytiotrophoblast. In the junctional zone between
subplacenta and decidua, there are nests of multinucleated giant cells with vacuolated cytoplasm.
The entire placenta rests on a pedicle of maternal tissue. An inverted yolk sac placenta is also
present. The presence of small vesicles and tubules in the apical membrane of the yolk sac
endoderm and larger vesicles in the supranuclear region suggest that the yolk sac placenta
participates in maternal-fetal transfer of protein.
Conclusion: The paca placenta closely resembles that of other hystricomorph rodents. The
lobulated structure allows for a larger exchange area and the development of precocial young.
Page 1 of 12
(page number not for citation purposes)
Introduction
The paca (Agouti paca, L) is a South American rodent that
lives in forested habitats near water and feeds largely on
fallen fruit. It is hunted for its meat, which is considered a
delicacy, and is an important source of animal protein for
rural populations. This has led to indiscriminate exploitation, resulting in a significant reduction in the population
density of this species in Brazil.
We here describe the morphology of paca placenta as
revealed by light microscopy and transmission electron
microscopy. This study is part of a wider effort to document the reproductive physiology of paca. It is hoped that
the information obtained will contribute to a rational
strategy for conservation of the species and possibly for
production, as paca has great potential as a commercial
food animal [1].
Materials and methods
The observations are based on placentae collected from 13
pregnant females. One was in early gestation, two in
midgestation and nine near term of pregnancy. This material was collected at Paulista State University, Jaboticabal,
Sao Paulo, Brazil. The research was authorized by the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA). The experimental protocol was
approved by the Bioethics Committee of the School of
Veterinary Medicine, University of Sao Paulo.
The animals were sedated with azaperone (Stresnil, Janssen Pharmaceutica, Brazil; 0.1 mg/kg I.M.) and given atropine (0.5 mg I.M.). Anaesthesia was induced with xylazine
(Coopazine, Coopers Brazil, Sao Paulo, S.P., Brazil; 1.5
mg/kg I.M.) and ketamine (Holliday Scott S.A., Brazil; 20
mg/kg I.M.). Hemihysterectomy was then performed
under aseptic conditions during inhalation anaesthesia
with halothane (Hoechst, Frankfurt, Germany). Postoperatively the animals were treated with benzyl penicillin and
streptomycin (Pentabiotico®, Fort Dodge, Campinas, S.P.,
Brazil; 8,000–24,000 IU/kg I.M.) and an analgetic
(buprenorphine, Temgesic®, Schering-Plough, S.P., Brazil). A detailed description of the anaesthesia and surgical
procedures has been published elsewhere [2].
Pieces of ten placentae were fixed in Bouin's solution or
10% formaldehyde and processed by standard histological procedures for embedding in paraplast, then sectioned
at 7 µm (automatic microtome, Model RM2155, Leica,
Germany). Sections were stained with haematoxylin and
eosin, Masson's trichrome or Gomori's trichrome or by
the periodic acid Schiff (PAS) reaction with haematoxylin
as counterstain.
http://www.rbej.com/content/3/1/9
hyede in 0.1 M phosphate buffer, pH 7.4, washed in
buffer and post-fixed in 1% osmium tetroxide (Polysciences, Warrington, PA, USA). They were then dehydrated, washed with propylene oxide and embedded in
Spurr's resin (Spurr's Kit, Electron Microscopy Sciences,
CO, U.S.A.). 60 nm sections were made and stained with
2% uranyl acetate (5 minutes) and 0.5% lead citrate (10
minutes). The ultrastructural observations were made
with a transmission electron microscope (JEOL 1010, Peabody, MA, U.S.A).
Results
The overall plan of the paca placenta is shown schematically in Figure 1. The labyrinth is divided into lobes separated by interlobular trophoblast. Beneath this is the
subplacenta, a structure unique to hystricomorph rodents.
The junctional zone between these structures and the
maternal decidua contains nests of giant cells. The placenta is attached to the uterus by a pedicle of maternal tissue. In addition, there is an inverted yolk sac placenta,
which connects with the fetal surface of the chorioallantoic placenta.
Histology
The centres of the lobes, the labyrinth and the interlobular
regions are clearly defined (Figure 2A). The central region
of each lobe contains fetal and maternal vessels around
which there is a considerable quantity of connective tissue
(fetal mesenchyme; Figure 2B). The vessels carrying
maternal arterial blood lack endothelium and they are
lined by trophoblast cells (Figure 2C).
The most extensive portion of the lobe is the labyrinth.
Due to close proximity between maternal and fetal blood
vessels, it is the region where most maternal-fetal
exchange takes place. The maternal blood spaces or lacunae are not lined by endothelium; they are defined by trophoblastic cell columns or cords. The cell columns are
radially arranged as is apparent when the lobe is seen in
cross section (Figure 2D). The syncytial nature of the trophoblastic columns is indicated by the close proximity of
their nuclei.
The interlobular regions comprise cords of syncytiotrophoblast with abundant basophilic cytoplasm. These
cords define maternal blood channels. The channels converge upon larger blood spaces, still without an endothelial lining, that receive blood from two or more adjacent
lobes. Thus, each interlobular region is common to several lobes (Figure 3A). The interlobular regions also contain fetal arteries (Figure 3B) that give rise to the
capillaries of the labyrinth.
Seven placentae were processed for transmission electron
microscopy. Small samples were fixed in 2.5% glutaralde-
Page 2 of 12
labyrinth
yolk sac
subplacenta
decidua
pedicle
Figure 1 drawing of the paca placenta
Schematic
Schematic drawing of the paca placenta. The labyrinth is divided into lobes separated by interlobular trophoblast. Beneath it is
found the subplacenta and then the decidua. There is a tenuous attachment to the uterine wall, the pedicle or mesoplacenta.
An inverted yolk sac placenta is present throughout gestation.
Placental surface
Most of the surface of the placental disk is covered by an
epithelium formed by the endoderm of the parietal yolk
sac (Figure 4A–C). An almost continuous Reichert's membrane can be demonstrated (Figure 4B). Beneath it is a
layer of spongiotrophoblast. These cells differ from those
that occur in the marginal and interlobular trophoblast.
They are larger in size and have a rounded and vacuolated
appearance (Figure 4C). The centre of the fetal surface of
the placenta, including the attachment of the cord, is covered by a layer of connective tissue (Figure 4D).
Subplacenta, junctional zone and pedicle
The subplacenta is organized as folded lamellae of
cytotrophoblasts supported on a thin layer of mesenchyme carrying fetal vessels (Figure 5A). The cytotrophoblast is multilaminar and mitotic figures are common here
in early and midgestation. Beneath this layer is syncytiotrophoblast, which contains vacuoles and PAS-positive
material. In late gestation this region becomes more compact and the entire subplacenta undergoes a process of
degeneration.
Groups of giant cells are found in the junctional zone
between the subplacenta and decidua (Figure 5B). They
are multinucleated and have a finely granular, basophilic
cytoplasm. They are PAS-positive.
The placenta is attached to the uterus by a placental pedicle made up of uterine tissue. In the upper region of this
pedicle, a fine and discontinuous layer of connective tissue is interposed between the maternal tissue and fetal
trophoblast. In the middle portion of the pedicle, a large
number of vessels pass to or from the placenta. This
Page 3 of 12
A
B
in
lab
cl
mes
fv
ma
lab
in
C
fv
tr
D
mes
mbs
fc
Figure
The
labyrinth
2
of the paca placenta
The labyrinth of the paca placenta. (A) The central region of a lobe (cl), a labyrinthine region (lab) and interlobular regions (in).
Haematoxylin and eosin. (B) Central region of a placental lobe, showing the presence of fetal veins (fv), maternal arterial blood
spaces (ma) lined by trophoblast cells, and the mesenchyme (mes) surrounding these structures. Haematoxylin and eosin. (C)
Detail to show the trophoblastic lining of maternal blood spaces (tr) and the intact walls of small fetal veins. PAS. (D) The placental labyrinth, showing the radial disposition (←) of the trophoblastic columns, the fetal capillaries (fc) and maternal blood
spaces (mbs). Haematoxylin and eosin. Scale bars: 500 µm (A), 200 µm (B); 50 µm (C, D).
region is characterized by dense fibres of connective tissue
externally and of looser connective tissue around the
vessels (Figure 5C). A layer of squamous epithelial cells
with simple, round nuclei, lightly condensed chromatin
and clear cytoplasm covers the entire pedicle (not shown).
Yolk Sac Placenta
There is an inverted yolk sac placenta, which is attached to
the fetal surface of the chorioallantoic placenta. Just
before attachment it forms the fibrovascular ring (Figure
4A). The yolk sac exhibits numerous digitiform projections (Figure 6A), which sometimes are branched. They
consist of a mesenchymal core covered by a layer of endoderm. The latter forms a simple columnar epithelium of
cells with apically situated cell nuclei (Figure 6B).
Ultrastructure
The paca placenta is of the syncytial haemomonochorial
type. A single trophoblast layer can be identified between
the blood in the maternal blood spaces of the labyrinth
and the endothelium of the fetal capillaries (Figure 7A–
B). This trophoblast is syncytial in nature without cell
boundaries and with large nuclei, often in close proximity
to one other. Microvilli project from the apical membrane
Page 4 of 12
A
cytotrophoblast cells as well as between cytotrophoblasts
and the overlying syncytium.
The cells of the parietal yolk sac endoderm form a columnar epithelium (Figure 7D). These cells are irregular in
shape with basally situated nuclei. The apical membrane,
which faces the uterine lumen, has microvilli and caveolae. The supranuclear cytoplasm contains vacuoles and
vesicles, tubular mitochondria and rough endoplasmic
reticulum. Desmosomes are found between the lateral
membranes of adjacent cells.
Subplacenta and junctional zone
The cytotrophoblast layer is multilaminar with dilated
intercellular spaces (Figure 8A). The cytoplasm of the
syncytium has mitochondria, rough endoplasmic reticulum, numerous electron-dense granules (Figure 8B) and
large accumulations of electron-dense material. The cytoplasm has electron transparent patches, which gives it a
vacuolated appearance. There are lacunae within the
syncytiotrophoblast, lined by microvilli and containing
material of moderate electron density (Figure 8B).
Desmosomes occur between adjacent cytotrophoblast
cells and between the plasma membranes of these cells
and that of the syncytial trophoblast.
Figure
The
interlobium
3
The interlobium of the paca placenta. (A) Channels in the
interlobium (in) drain the maternal blood spaces of the labyrinth (lab) and converge on larger venous blood spaces (mv).
Haematoxylin and eosin. (B) Fetal artery (fa) at the border
between an interlobular region and the labyrinth at the
periphery of a lobe. Haematoxylin and eosin. Scale bars: 100
µm (A); 50 µm (B).
into the maternal blood space. Caveolae are seen in the
apical membrane and the syncytiotrophoblast contains
coated vesicles and larger vacuoles. There are recesses in
the basal membrane. However, we saw no evidence of
transtrophoblastic channels. There is an abundant
amount of rough endoplasmic reticulum, a Golgi apparatus, lysosomes and numerous mitochondria.
In the junctional zone between the decidua and the lateral
aspect of the subplacenta, there are nests of multinucleated giant cells (Figure 8C). Their morphology is variable.
The cytoplasm has extensive electron transparent areas.
The organelles tend to be confined to the perinuclear and
marginal areas (Figure 8D) and include mitochondria,
rough endoplasmic reticulum and electron-dense granules. The giant cells are separated by electron-dense material into which they send processes (Figure 8D).
Yolk sac placenta
The apical surface of the endoderm cells has numerous
microvilli of relatively uniform length (Figure 9A). Small
vesicles and tubules are present in the most apical regions
of the cytoplasm (Figure 9B). The supranuclear cytoplasm
contains a number of larger vesicles and vacuoles with a
variable amount of electron-dense content. The perinuclear cytoplasm also houses a small Golgi complex. The
cytoplasm has mitochondria and rough endoplasmic
reticulum. Desmosomes and terminal bars are present
between the lateral membranes of the cells.
Discussion
In the interlobular areas, the syncytiotrophoblast bordering the maternal blood spaces has numerous microvilli
(Figure 7C). The cytoplasm has abundant rough endoplasmic reticulum, mitochondria and electron-dense
droplets. Cytotrophoblast cells occur within the
syncytium. Desmosomes are present between adjacent
As in other hystricomorph rodents [3,4], the placenta of
paca consists of several lobes separated by interlobular
trophoblast. The center of each lobe contains maternal
arteries from which blood flows to the periphery through
the trophoblastic channels of the labyrinth. In the fetal
capillaries, blood flows from the periphery towards the
Page 5 of 12
D
Figure
Fetal
surface
4
Fetal surface of the paca placenta. (A) The visceral yolk sac (vys) attaches to the surface of the chorioallantoic placenta. Just
before attachment it forms the fibrovascular ring (fvr). Left of the point of attachment, the endoderm continues as the parietal
yolk sac (pys). To the right, the surface is covered by connective tissue. Masson's trichrome. (B) The parietal yolk sac endoderm (endo) forms a layer of epithelial cells that rests on Reichert's membrane (Rm). Immediately below the membrane are
scattered connective tissue cells (ct). Masson's trichrome. (C) Beneath the endoderm and Reichert's membrane are spongiotrophoblast cells (sp tr), with a vacuolated appearance, marginal syncytium (ma tr) and a portion of the labyrinth (lab). Haematoxylin and eosin. (D) The centre of the placental disk is covered by connective tissue. Beneath this are marginal trophoblast
and labyrinth. Haematoxylin and eosin. Scale bars: 500 µm (A); 10 µm (B); 100 µm (C-D).
Page 6 of 12
A
center, allowing for countercurrent exchange [5,6]. The
interlobular regions are made up of cords of syncytiotrophoblast, which define maternal blood spaces. We show
here that each interlobular region drains several lobes.
fm
cy tr
sy tr
B
In the labyrinth, the trophoblast is bathed directly by
maternal blood and is separated from the fetal capillaries
by a single layer of syncytiotrophoblast. Thus the placental barrier is syncytial haemomonochorial, as in the
guinea pig [7-9], chinchilla [10], cane rat [11], degu [12]
and rock cavy [13]. The apical membrane of this trophoblast, which is in contact with maternal blood, is well
supplied with microvilli. There are recesses in the basal
membrane and caveolae can occasionally be seen at the
apical membrane. However, we did not observe
transtrophoblastic channels such as those described in the
degu [12].
In the interlobular region, the trophoblast contained
mitochondria and rough endoplasmic reticulum. The
surface in contact with maternal blood bore numerous
microvilli. The interlobular trophoblast is the functional
equivalent of the spongy zone of murid rodents [14]. In
the guinea pig it has been identified as the principal site of
progesterone synthesis [15]. In addition, it is thought to
synthesize progesterone-binding protein [16], which is
found in the plasma throughout gestation and is unique
to hystricomorph rodents.
C
ct
mbv
Figure 5 junctional zone and pedicle of the paca placenta
Subplacenta,
Subplacenta, junctional zone and pedicle of the paca placenta.
(A) Subplacenta. A layer of cytotrophoblasts (cy tr) is supported on lamellae of fetal mesenchyme (fm). Beneath it is
the subplacental syncytiotrophoblast (sy tr). Gomori's trichrome. (B) Groups of multinucleated giant cells with a finely
granular cytoplasm are found between the subplacenta and
decidua. They are bordered by connective tissue. Masson's
trichrome. (C) Middle portion of the placental pedicle, showing a large number of maternal blood vessels (mbv) and connective tissue fibers (ct). Haematoxylin and eosin. Scale bars:
20 µm (A-B); 200 µm (C).
Much of the surface of the placental disk is covered by the
endoderm of the parietal yolk sac. This epithelium is
largely columnar and rests on Reichert's membrane.
Beneath the membrane are trophoblast cells that differ
from those in other regions of the placenta in their larger
size, rounder form and vacuolated appearance. An appropriate designation for these cells is spongiotrophoblast. It
has been shown in the guinea pig that maternal protein
can cross the spongiotrophoblast and Reichert's membrane. It can then pass into the uterine lumen through the
intercellular spaces between the endoderm cells, as they
are not sealed by tight junctions [17]. In theory the
protein could then be taken up by the visceral yolk sac,
but whether maternal-fetal exchange occurs by this circuitous route is open to speculation.
The subplacenta is a unique feature of hystricomorph
rodents [3]. Characteristic of the subplacenta of paca were
the large intercellular spaces between the cytotrophoblasts
and the lacunae within the syncytiotrophoblast. As in the
guinea pig [18] and chinchilla [10], the lacunae in the
syncytium were lined by microvilli and contained electron-dense material. It seems likely that the lacunae intercommunicate, but this requires further investigation.
Wolfer and Kaufmann [19] suggested that the subplacenta
might be a highly active area from a metabolic point of
Page 7 of 12
A
Figure
Yolk
sac6placenta of the paca
Yolk sac placenta of the paca. (A) The visceral yolk sac is complexly folded with columnar epithelial cells of endodermal origin
(endo) supported by fetal mesenchyme (fm). Haematoxylin and eosin. (B) The mesenchyme (stained blue) contains vitelline
blood vessels (vit bv). Masson's trichrome. Scale bars: 50 µm (A); 10 µm (B).
view. They pointed out that the structure had been carefully described, but that little was known about its function, except that it might have endocrine activity. Recently
it was proposed that the subplacenta is an important
source of invasive trophoblast in the guinea pig, chinchilla, capybara and degu [20].
We found multinucleated giant cells in the junctional
zone between the subplacenta and decidua. Intriguingly,
the cytoplasm of these cells contained electron-dense
granules reminiscent of those found in the subplacental
syncytium. The cytoplasm of the giant cells had areas of
low electron density, a feature also shared by the subplacental syncytium. These cells were PAS-positive and may
store glycogen or glycoprotein.
The placenta of paca is attached to the uterus by a prominent structure, formed largely of maternal tissue, that we
have denoted the placental pedicle. It was first described
by Strahl [21] and named by him the mesoplacenta. A
similar structure occurs in the agouti [4], chinchilla [22]
and nutria [5]. The equivalent formation in the capybara
and guinea pig placenta is the placental stalk [23]. Trophoblast is found in the walls of the maternal vessels that
pass through the pedicle to supply the placenta [4].
Like other hystricomorph rodents, paca has an inverted
yolk sac placenta that persists until term. This visceral yolk
sac displays folds and complex villi. The numerous
digitiform projections are sometimes branched. They consist of a mesenchymal axis covered by a simple columnar
epithelium of endodermal cells. The cells seem to have a
Page 8 of 12
A
B
mbs
mbs
Ÿ
Ÿ
cv
fc
fc
C
D
cy tr
sy tr
mbs
Figure 7
Ultrastructure
of the labyrinth, interlobium and parietal yolk sac endoderm
Ultrastructure of the labyrinth, interlobium and parietal yolk sac endoderm. (A-B) The interhaemal barrier. Only a single layer
of syncytiotrophoblast is interposed between the blood flowing in the maternal blood spaces (mbs) and the endothelium of the
fetal capillary (fc). The apical membrane contains invaginations (arrowheads) and the cytoplasm includes small coated vesicles
(cv) and larger vacuoles. There are recesses in the basal membrane (arrows). (C) Interlobium. Most of the trophoblast is syncytial (sy tr) with abundant rough endoplasmatic reticulum. There are many microvilli where it is in contact with the maternal
blood space. Cytotrophoblast cells with large nuclei are found in some regions of the interlobium. Desmosomes are found
between the lateral membranes of adjacent cells (arrowheads). (D) Parietal yolk sac endoderm. These columnar cells have
numerous microvilli at the apical surface. The supranuclear cytoplasm contains vacuoles and vesicles, tubular mitochondria and
rough endoplasmic reticulum. Desmosomes are found between the lateral membranes of adjacent cells (arrowheads). Scale
bars: 1 µm (A-B); 5 µm (C); 2 µm (D).
Page 9 of 12
A
B
cy tr
sy tr
dd
cy tr
sy tr
bm
C
D
gc
gc
Figure 8
Ultrastructure
of the subplacenta and junctional zone of the paca placenta
Ultrastructure of the subplacenta and junctional zone of the paca placenta. (A) The cytotrophoblast layer (cy tr) is multilaminar
with dilated intercellular spaces. The cells are characterized by their large nuclei. They rest on a thin basement membrane (bm)
which separates them from the fetal mesenchyme. (B) The syncytiotrophoblast (sy tr) contains electron-dense droplets (dd).
Microvilli project from the syncytiotrophoblast into lacunae containing material of moderate electron density (arrows). (C)
Multinucleated giant cells from the junctional zone. The cytoplasm has electron transparent areas, giving it a vacuolated appearance. (D) Two giant cells (gc) separated by intercellular matrix into which they send processes (arrows). Scale bars: 5 µm (AC); 1 µm (D).
Page 10 of 12
A
B
Ÿ
Ÿ
cv
cv
Figure 9
Ultrastructure
of the inverted yolk sac placenta of the paca
Ultrastructure of the inverted yolk sac placenta of the paca. (A) The apical surface of the endodermal cells bears numerous
microvilli. The supranuclear cytoplasm contains many larger vesicles or vacuoles with a small amount of electron dense content. (B) Invaginations (arrowheads), small coated vesicles (cv) and tubules are present in the most apical regions of the cytoplasm. Scale bars: 4 µm (A); 1 µm (B).
high level of endocytotic activity. Similar characteristics
are found in the yolk sac endoderm of the guinea pig [24],
chinchilla [10] and rock cavy [13]. In the guinea pig it has
been shown experimentally that immunoglobulin G is
taken up from the uterine lumen to coated pits. The endocytotic vesicles thus formed are transported to the lateral
membrane and empty into the intercellular spaces by exocytosis [25]. From here the immunoglobulins are presumed to reach fetal capillaries. Protein cannot move
directly into the intercellular spaces because of the tight
junctions near the apex of the cells [25]. In addition to this
mechanism for conferring passive immunity to the fetus,
there is nonspecific uptake of protein from the uterine
lumen. Many endocytotic vesicles fuse with larger vacuoles that form part of the cell's lysosomal apparatus [26].
The protein they contain is thought to provide amino
acids to the fetus. Given the similarity in ultrastructure,
these mechanisms are likely to operate in the yolk sac placenta of paca.
In conclusion, the placenta of the paca conforms to patterns previously described for hystricomorph rodents
[3,14]. Common features include the lobulation of the
placenta and the presence of a subplacenta. At the
ultrastructural level they comprise the haemomonochorial nature of the interhaemal barrier and the pinocytotic
apparatus of the visceral yolk sac endoderm. The lobulated structure of the placenta allows for a larger exchange
area and the development of precocial young [14].
Recently it was argued that more attention should be
given to the hystricomorph rodents as models in human
medicine. They bear a closer genetic similarity to humans
than do murid rodents, such as the mouse and rat,
Page 11 of 12
because the latter have undergone a very high rate of gene
mutation [27]. Since the paca carries a singleton fetus with
a birth weight of 640–900 g, it deserves particular consideration as a potential model of fetal growth and development [28].
18.
Acknowledgements
20.
This study was supported by Fundação de Amparo à Pesquisa do Estado de
São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico
e Tecnológico (CNPq). We are grateful to Dr. Fabrício Singaretti de
Oliveira (UNESP) for ultrasound examination of the animals. Marina
Bonatelli wishes to thank Professors José Manoel dos Santos (FM-ABC),
Idercio Luiz Sinhorini (USP) and Áureo Tatsumi Yamada (UNICAMP) for
their guidance.
21.
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Placentation in the paca (Agouti paca L) - BDPI USP

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